Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes Ben L. Phillips* and Richard Shine School of Biological Sciences A08, University of Sydney, New South Wales 2006, Australia Edited by David B. Wake, University of California, Berkeley, CA, and approved October 27, 2004 (received for review August 31, 2004) The arrival of invasive species can devastate natural ecosystems, much less research has been conducted on counteradaptations but the long-term effects of invasion are less clear. If native by native species (17, 18). organisms can adapt to the presence of the invader, the severity of Many species of Australian snake have been severely impacted impact will decline with time. In Australia, invasive cane toads by the invasion of highly toxic cane toads (Bufo marinus), a (Bufo marinus) are highly toxic to most snakes that attempt to eat conservation problem that also offers an ideal situation to them. Because snakes are gape-limited predators with strong explore the possibility of an adaptive response by natives to an negative allometry for head size, maximum relative prey mass (and invader. Cane toads were introduced into Australia in 1935. thus, the probability of eating a toad large enough to be fatal) Since then, they have spread throughout large areas of Queens- decreases with an increase in snake body size. Thus, the arrival of land and have entered the Northern Territory and New South Ϸ 2 toads should exert selection on snake morphology, favoring an Wales, currently occupying a range of 1 million km (19). The ecological impact of toads on the native fauna has been poorly increase in mean body size and a decrease in relative head size. We elucidated, mainly because of logistical difficulties and a lack of tested these predictions with data from specimens of four species baseline data for comparison (20). Nevertheless, there is a clear of Australian snakes, collected over >80 years. Geographic infor- inference that the invasion of the toad has had a massive impact mation system layers provided data on the duration of toad on species of Australian snakes. Toads are highly toxic, and most exposure for each snake population, as well as environmental Australian snakes attempting to eat toads will die. A recent study variables (latitude, precipitation, and temperature). As predicted, suggests that 49 species of snake are potentially impacted by the two toad-vulnerable species (Pseudechis porphyriacus and Den- toad and that the majority of these species are unable to deal with drelaphis punctulatus) showed a steady reduction in gape size and a likely dose of toad toxin (21). a steady increase in body length with time since exposure to toads. However, snakes are gape-limited predators and, thus, their In contrast, two species at low risk from toads (Hemiaspis signata ability to poison themselves by consuming a toad depends on and Tropidonophis mairii) showed no consistent change in these their head size (HS) relative to their body mass. Thus, within any morphological traits as a function of the duration of toad exposure. given population, a snake with a small head relative to its body These results provide strong evidence of adaptive changes in mass will be at less risk of ingesting a toad large enough to kill native predators as a result of the invasion of toxic prey. it than will a conspecific capable of ingesting a relatively larger toad. At an intraspecific level, two major factors influence the adaptation ͉ conservation ͉ contemporary evolution ͉ coevolution size of a snake’s head relative to body mass: the snake’s absolute size (because smaller individuals have relatively larger heads, as is generally true in most vertebrates; ref. 22) and relative HS uman-induced environmental change is the greatest threat (because even at the same body length, some individuals will Hto global biodiversity. Such processes include global climate have larger heads than will others). Thus, the risk of a snake change, invasive species, habitat removal, overharvesting, and consuming a toad large enough to be fatal will depend on snake altered biogeochemical cycles (1–3). These changes have caused body size and relative HS (unpublished data). Accordingly, we many extinctions (local and global) and will lead to many more, expect that the arrival of toads will impose selection on the but whenever the impact is nonrandom (i.e., selective), there is morphology of snakes, favoring individuals with larger-than- the potential for adaptive evolution. Under the right circum- average body sizes and smaller-than-average relative HS. stances, adaptive evolution can happen very rapidly in wild In this study, we examine morphological variation in four populations. Such ‘‘contemporary evolution’’ (see ref. 4) occurs species of Australian snakes. Two of these taxa (one colubrid, as a consequence of selection during natural events (e.g., refs. one elapid) are predicted to face little to no impact from toads, 5–7). Importantly, however, it has also been documented from either because they are too small to ingest a fatal dose or because ‘‘unnatural’’ (human-mediated) events. The classic example of they have high physiological resistance to toad toxins. The other industrial melanism in peppered moths is the most celebrated two taxa (again, one colubrid and one elapid) are predicted to case (8, 9); however, there is also clear evidence of adaptive be much more vulnerable to toad invasion. We examine variation evolution in populations as a consequence of overfishing (10), in body size and relative HS with reference to environmental global warming (11), and heavy-metal pollution (12). variables and time since exposure to toads. We predict that mean body sizes and͞or relative HSs will have changed through time These studies highlight the importance of examining the since toad arrival in the toad-vulnerable species, but not in the potential for adaptive change in impacted populations. Doing so other taxa. can clarify both the nature of the impact and the response of the affected population. Clearly, a population exhibiting an adaptive Methods response is more likely to persist in the face of an environmental Study Species and Collection of Morphological Data. To ensure change than one that fails to adapt. Invasive species are of phylogenetic independence, we selected distantly related taxa particular interest in this respect because they are believed to constitute a major threat to global biodiversity (3, 13, 14). Although invasive species have caused extinctions (e.g., refs. 15 This paper was submitted directly (Track II) to the PNAS office. and 16) they may also exert nonrandom selection upon impacted Abbreviations: HS, head size; SVL, snout-vent length; GIS, geographic information system; species, such that natives can adapt to their presence. Although ET, exposure time; PCn, principal component n. much evolutionary research has been directed toward invasive *To whom correspondence should be addressed. E-mail: [email protected]. species themselves and how they adapt to new environments, © 2004 by The National Academy of Sciences of the USA 17150–17155 ͉ PNAS ͉ December 7, 2004 ͉ vol. 101 ͉ no. 49 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0406440101 Downloaded by guest on October 2, 2021 within each of our two categories (vulnerable and nonvulnerable species). All four study species feed primarily or exclusively on anurans, and are widely distributed through the parts of Queens- land invaded by cane toads since 1935. The two highly vulnerable taxa comprised red-bellied blacksnakes (Pseudechis porphyria- cus, Elapidae, n ϭ 99) and green tree snakes (Dendrelaphis punctulatus, Colubridae, n ϭ 242). Like most Australian snake species, these snakes are highly susceptible to toad toxins, and will die if they ingest even a relatively small toad. To consume a fatal dose of toxin, Pseudechis needs only to consume a toad whose head width is 43% of its own, and Dendrelaphis needs only consume a toad whose head width is 49% of its own (21). The two relatively nonvulnerable species were swamp snakes (Hemi- aspis signata, Elapidae, n ϭ 158) and keelbacks (Tropidonophis mairii, Colubridae, n ϭ 124). These two taxa are less likely to be severely impacted by cane toads. Hemiaspis is a small species with an unusually small head, and hence consumes only very small anurans, even relative to its own body mass; to consume a fatal dose it would need to ingest a toad that is 108% of its head-width (21). In contrast, Tropidonophis is a larger species with a normal-sized head, but has an unusually high physiological tolerance for toad toxins; to consume a fatal dose, this species would need to consume a toad that is 185% of its head-width, and so feeds readily on toads without severe ill effects (21, 23). Fig. 1. GIS layer describing the timing of the cane toad invasion in Queens- We collected morphological data from preserved specimens land, Australia. The extreme western edge of the distribution follows the held at the Queensland Museum. Toads have populated Ͼ60% extent of distribution records in Queensland and may not accurately reflect of Queensland, and all sampled animals came from areas where the actual invasion extent. Data are from Floyd et al. (26) and the specimen toads have colonized. We sampled the entire specimen collec- register of the Queensland Museum. tion for each of our species, except Tropidonophis (for which we Ϸ took a random sample amounting to 50% of the entire plotted toad locality data and identified the earliest record of collection for the species). Thus, our sampling spanned the entire toads at each site by cumulatively stepping through the data set known geographic range of each species in Queensland. We at 2-year intervals beginning at 1935 (the year that toads were selected these taxa based on their wide phylogenetic separation, released in Queensland).